Checking the pulse of Lake Ontario's microbial-planktonic communities: A trophic transfer hypothesis
Keywords:
lower trophic levels, linkages, food web, carbon dynamics, fisheriesAbstract
The structure and function of the microbial food web of Lake Ontario was assessed at 15 stations distributed across 4 transects during the spring and summer of 2003. This was the first major binational study of Lake Ontario since the Lake Ontario Trophic Transfer initiative of 1990. The microbial loop (bacteria, autotrophic picoplankton, heterotrophic nanoflagellates (HNF) and ciliates) and phytoplankton, were enumerated microscopically in addition to measurements of chlorophyll a, size fractionated primary productivity (14C) and bacterial growth (3H). HNF dominated the total biomass in spring (≈300 mg m−3) and summer (≈1250 mg m−3). The size of the organic carbon pool increased from ≈90 mg C m−3 in spring to ≈270 mg C m−3 with HNF contributing 36% of the total organic carbon in the spring and 52% in the summer; however the net balance of the organic carbon pool shifted from autotrophic in the spring to heterotrophic in the summer. The available evidence suggests that HNF are a poor quality food resource for zooplankton and it is likely that the carbon sequestered by HNF is not available to higher trophic levels resulting in dietary stress for planktivores. The implications of high HNF for both organic carbon cycling and maintaining healthy fisheries needs further research. Independent observations show that oligotrophic conditions prevail as evidenced by low phosphorus, low chlorophyll a, low plankton and high water clarity. Such conditions have been generally regarded as the gold standard for managing healthy lakes. Lake Ontario is oligotrophic and healthy from a water quality perspective, but from a food web dynamics point of view, Lake Ontario appears to be unhealthy due to the dominance of HNF, low zooplankton and poor quality of food available to higher trophic levels. We hypothesize that the lake's poor health is attributable to inefficient energy transfer from lower to higher trophic levels. The traditional understanding of trophic state based mainly on water quality criteria needs to be broadened by the inclusion of food web and fisheries based metrics.
References
Anderson, T. and Hessen, D. O. 1991. Carbon, nitrogen and phosphorus content of freshwater zooplankton. Limnol. Oceanogr., 36: 807–813.
Biddanda, B., Ogdahl, M. and Cotner, J. 2001. Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol. Oceanogr., 46(3): 730–739.
Bocaniov, S. A. and Smith, R. E. H. 2009. Plankton metabolic balance at the margins of very large lakes: temporal variability and evidence for dominance of autochthonous processes. Freshwater Biology, 54: 345–362.
Brett, M. T., Kainz, M. J., Taipale, S. J. and Seshan, H. 2009. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. PNAS, 106(50): 21197–21201.
Carrick, H. J., Fahnenstiel, G. L. and Taylor, W. D. 1992. Growth and production of planktonic protozoa in Lake Michigan: in situ versus in vitro comparisons and importance to food web dynamics. Limnol. Oceanogr., 37(6): 1221–1235.
Cotner, J., Biddanda, B., Makino, W. and Stets, E. 2004. Organic carbon biogeochemistry of Lake Superior. Aquat. Ecosyst. Health Mgmt., 7(4): 451–464.
del Giorgio, P. A. and Peters, R. H. 1994. Patterns in planktonic P:R ratios in lakes: influence of lake trophy and dissolved organic carbon. Limnol. Oceanogr., 39: 772–787.
Dodds, W. K. and Cole, J. J. 2007. Expanding the concept of trophic state in aquatic ecosystems: it's not just the autotrophs. Aquat. Sci., 69: 427–439.
Dove, A. 2009. Long-term trends in major ions and nutrients in Lake Ontario. Aquat. Ecosyst. Health. Mgmt., 12(3): 281–295.
Environment Canada and United States Environmental Protection Agency. 1995. The Great Lakes: an environmental atlas and resource book, , 3rd Edition http://www.epa.gov/glnpo/atlas/index.html. Last accessed: December 2, 2009
Fahnenstiel, G. L., Krausse, A. E., McCormick, M. J., Carrick, H. J. and Schelske, C. L. 1998. The structure of the planktonic food web in the St. Lawrence Great Lakes. J. Great Lakes Res., 24: 531–554.
Fitzpatrick, M. A. J., Munawar, M. and Haffner, G. D. 2008. “Application of the primary production required model for managing the commercial fisheries in western Lake Erie”. In Checking the pulse of Lake Erie, Edited by: Munawar, M. and Heath, R. T. 475–495. Burlington, ON: Ecovision World Monograph Series. Aquatic Ecosystem Health and Management Society.
Haffner, G. D., Yallop, M. L. and Hebert, P. D. N. 1988. Heterotrophic glucose assimilation in Lake Ontario. J. Great Lakes Res., 14(2): 157–163.
Heath, R. T. and Munawar, M. 2004. Bacterial productivity in Lake Superior, 2001: implications for food web efficiencies in oligotrophic freshwater ecosystems. Aquat. Ecosyst. Health. Mgmt., 7(4): 465–474.
Heath, R. T., Hwang, S. J. and Munawar, M. 2003. A hypothesis for the assessment of the importance of microbial food web linkages in nearshore and offshore habitats of the Laurentian Great Lakes. Aquat. Ecosyst. Health. Mgmt., 6(3): 231–239.
Hiriart-Baer, V. P., Diep, N. and Smith, R. E. H. 2008. Dissolved organic matter in the Great Lakes: role and nature of allocthonous material. J. Great Lakes Res., 34: 383–394.
Holeck, K. T., Watkins, J. M., Mills, E. L., Johannsson, O., Millard, S. and Richardson, V. 2008. Spatial and temporal long term assessment of Lake Ontario water clarity, nutrients, chlorophyll a, and zooplankton. Aquat. Ecosyst. Health. Mgmt., 11(4): 377–391.
Hwang, S-J. and Heath, R. T. 1997. Bacterial productivity and protistan bacterivory in coastal and offshore communities of Lake Erie. Can. J. Fish. Aquat. Sci., 54: 788–799.
Hwang, S-J. and Heath, R. T. 1999. Zooplankton bacterivory at coastal and offshore sites of Lake Erie. J. Plankton Res., 21(4): 699–719.
Ivanikova, N. V., McKay, R. M. L., Bullerjahn, G. S. and Sterner, R. W. 2007. Nitrate utilization by phytoplankton in Lake Superior is impaired by low nutrient (P, Fe) availability and seasonal light limitation—a cyanobacterial bioreporter study. J. Phycol., 43: 475–484.
Jørgensen, N. O. G. 1992. Incorporation of [3H]leucine and [3H]valine into protein of freshwater bacteria: field applications. Appl. Environ. Microbiol., 58: 3647–3653.
Leach, J. H., Dickie, L. M., Shuter, B. J., Borgmann, U., Hyman, J. and Lysack, W. 1987. A review of methods for prediction of potential fish production with application to the Great Lakes and Lake Winnipeg. Can. J. Fish. Aquat. Sci., 44(Suppl. 2): 471–485.
Lee, S. and Fuhrman, J. A. 1987. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Env. Microbiol., 53: 1298–1303.
Lynn, D. H. and Munawar, M. 1999. “Abundance, biomass, and diversity of planktonic ciliates (Ciliophora) in Lake Erie”. In State of Lake Erie (SOLE)—past, present and future, Edited by: Munawar, M., Edsall, T. and Munawar, I. F. 155–168. Leiden, , Netherlands: Backhuys Publishers.
Mills, E. L., Casselman, J. M., Dermott, R., Fitzsimons, J. D., Gal, G., Holeck, K. T., Hoyle, J. A., Johannsson, O. E., Lantry, B. F., Makarewicz, J. C., Millard, E. S., Munawar, I. F., Munawar, M., O’Gorman, R., Owens, R. W., Rudstam, L. G., Schaner, T. and Stewart, T. J. 2003. Lake Ontario: Food web dynamics in a changing ecosystem (1970–2000). Can. J. Fish. Aquat. Sci., 60: 471–490.
Montagnes, D. J.S. and Lynn, D. H. 1993. “A quantitative protargol stain (QPS) for ciliates and other protists”. In Handbook of methods in aquatic microbial ecology, Edited by: Kemp, P. F., Sherr, B. F., Sherr, E. B. and Cole, E. J. 229–240. Boca Raton, FL: Lewis Publishers.
Munawar, I. F and Munawar, M. 2009. “Phytoplankton communities of Lake Superior, 2001: Changing species composition and biodiversity of a pristine ecosystem”. In State of Lake Superior, Edited by: Munawar, M. and Munawar, I. F. 319–359. Burlington, ON: Ecovision World Monograph Series, Aquatic Ecosystem Health and Management Society.
Munawar, M. 2003. “Editorial”. In State of Lake Ontario: past, present and future, Edited by: Munawar, M. xi–xiii. Burlington, Ontario: EcovisionWorld Monograph Series, Aquatic Ecosystem Health and Management Society.
Munawar, M. and Nauwerck, A. 1971. The composition and horizontal distribution of phytoplankton in Lake Ontario during the year 1970. Proc. 14th Conf. Great Lakes Res. Internat. Assoc. Great Lakes Res., : 69–78.
Munawar, M. and Munawar, I. F. 1982. Phycological studies in Lakes Ontario, Erie, Huron and Superior. Can. J. Bot., 60: 1837–1858.
Munawar, M. and Weisse, T. 1989. Is the ‘microbial loop’ an early indicator of anthropogenic stress?. Hydrobiol., 188/189: 163–174.
Munawar, M. and Munawar, I. F. 1996. Phytoplankton dynamics in the North American Great Lakes Vol. I: Lakes Ontario, Erie and St. Clair, Amsterdam: SPB Academic Publishing. Ecovision World Monograph Series
Munawar, M. and Munawar, I. F. 2000. Phytoplankton dynamics of the North American Great Lakes., Vol. 2, Leiden, , Netherlands: Backhuys Publishers.
Munawar, M. and Munawar, I. F. 2003. “Changes in the phytoplankton community structure and primary production of Lake Ontario”. In State of Lake Ontario: past, present and future, Edited by: Munawar, M. 187–219. Burlington, Ontario: Ecovision World Monograph Series, Aquatic Ecosystem Health and Management Society.
Munawar, M., Munawar, I. F., Culp, L. R. and Dupuis, G. 1978. Relative importance of nanoplankton in Lake Superior phytoplankton biomass and community metabolism. J. Great Lakes Res., 4(3–4): 462–480.
Munawar, M., Munawar, I. F., Norwood, W. P. and Mayfield, C. I. 1987a. Significance of autotrophic picoplankton in the Great Lakes and their use as early indicators of contaminant stress. Arch.Hydrobiol. Beih., 25: 141–155.
Munawar, M., Munawar, I. F. and McCarthy, L. 1987b. Phytoplankton ecology of large eutrophic and oligotrophic lakes of North America: Lakes Ontario and Superior. Arch. Hydrobiol. Bieh. Ergebn.Limnol., 25: 51–96.
Munawar, M., Munawar, I. F., Weisse, T., van Stam, H., Fitzpatrick, M. and Lorimer, L. 1999. “Probing microbial food-web structure in Lake Erie”. In State of Lake Erie (SOLE)—Past, Present and Future, Edited by: Munawar, M., Edsall, T. and Munawar, I. F. 197–218. Leiden, , Netherlands: Backhuys Publishers.
Munawar, M., Legner, M. and Munawar, I. F. 2003. “Assessing the microbial food web of Lake Ontario”. In State of Lake Ontario: past, present and future, Edited by: Munawar, M. 135–170. Burlington, Ontario: Ecovision World Monograph Series, Aquatic Ecosystem Health and Management Society.
Munawar, M., Munawar, I. F., Mandrak, N., Fitzpatrick, M., Dermott, R. and Leach, J. 2005. An overview of the impact of non-indigenous species on the food web integrity of North American Great Lakes: Lake Erie example. Aquat. Ecosyst. Health Mgmt., 8(4): 375–396.
Munawar, M., Munawar, I. F., Fitzpatrick, M., Niblock, H. and Lorimer, J. 2009. “The base of the food web at the top of the Great Lakes: structure and function of the microbial food web of Lake Superior”. In State of Lake Superior, Edited by: Munawar, M. and Munawar, I. F. 289–318. Burlington, ON: Ecovision World Monograph Series, Aquatic Ecosystem Health and Management Society.
O’Gorman, R., Prindle, S. E., Lantry, J. R. and Lantry, B. F. 2008. Distribution of the Lower Food Web in Lake Ontario: Did it affect Alewife Growth or Condition?. Aquat. Ecosyst. Health Mgmt., 11(4): 392–402.
Pace, M. L. 1993. “Heterotrophic microbial processes”. In The trophic cascade in lakes, Edited by: Carpenter, S. R. and Kitchell, J. F. 252–277. Cambridge, , UK: Cambridge University Press.
Pick, F. R. and Caron, D. A. 1987. Picoplankton and nanoplankton biomass in Lake Ontario: relative contribution of phototrophic and heterotrophic communities. Can. J. Fish. Aquat. Sci., 44(12): 2164–2172.
Porter, K. G. 1996. “Integrating the microbial loop and the classic food chanin into a planktonic food web”. In Food webs: integration of patterns and dynamics, Edited by: Polis, G. A. and Winemiller, K. O. 51–59. Boston, MA: Kluwer Academic Publishers.
Porter, K. G. and Feig, Y. S. 1980. The use of DAPI for identification and enumeration of bacteria and blue-green algae. Limnol. Oceanogr., 25: 943–948.
Pomeroy, L. R. 1974. The ocean's food web a changing paradigm. BioScience, 24: 499–504.
Reynolds, C. S., Reynolds, S. N., Munawar, I. F. and Munawar, M. 2000. The regulation of phytoplankton dynamics in the world's largest lakes. Aquat. Ecosyst. Health Mgmt., 3(1): 1–22.
Schroeder, R. 1969. Ein summierender wasserschopfer (An integrating water sampler. In German). Arch. Hydrobiol., 66: 241–243.
Schlectriem, C., Arts, M. T. and Johannsson, O. E. 2008. Effects of long term fasting on the use of fatty acids as trophic markers in the opossum shrimp Mysis relicta—a laboratory study. J. Great Lakes Res., 34: 143–152.
Sherr, E. B., Sherr, B. F. and Paffenhoefer, G.-A. 1986. Phagotrophic protozoa as food for metazoans: a ‘missing’ trophic link in marine pelagic food webs?. Mar. Microb. Food Webs, 1: 61–80.
Sherr, E. B., Sherr, B. F. and Hopkinson, C. S. 1988. Trophic interactions within pelagic microbial communities: indications of feedback regulation of carbon flow. Hydrobiologia, 159: 19–26.
Sprules, W. G., Johannsson, O. E., Millard, E. S., Munawar, M., Stewart, T. S., Tyler, J., Dermott, R., Whipple, S. J., Legner, M., Morris, T. J., Ghan, D. and Jech, J. M. Trophic transfer in Lake Erie: A whole food web modeling perspective. A White Paper Submitted for the Great Lakes Modeling Summit. 1999 May 24–28. 42nd Conference of the International Association of Great Lakes Research. Cleveland, OH.
Stewart, T. J., Sprules, W. G. and O’Gorman, R. 2009. Shifts in the diet of Lake Ontario alewife in response to ecosystem change. J. Great Lakes Res., 35: 241–249.
Strathman, R. R. 1967. Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol. Oceanogr., 12: 411–418.
Strickland, J. D.H. and Parsons, T. R. 1968. A practical handbook of seawater analysis, Ottawa, ON: Bulletin of the Fisheries Research Board of Canada.
Tadonléké, R. D., Pinel-Alloul, B., Bourbonnais, N. and Pick, F. R. 2004. Factors affectong the bacteria—heterotrophic nanoflagellate relationship in oligo-mesotrophic lakes. J. Plankton Res., 26(2): 681–695.
Turley, C. M., Newell, R. C. and Robins, D. B. 1986. Survival strategies of two small marine ciliates and their role in regulating bacterial community structure under experimental conditions. Mar. Ecol. Prog. Ser., 33: 59–70.
Urban, N. R., Auer, M. T., Green, S. A., Lu, X., Apul, D. S., Powell, K. D. and Bub, L. 2005. Carbon cycling in Lake Superior. J. Geophys. Res. C. Oceans, 110(6): 1–17.
Utermöhl, H. 1958. Zur vervolkommnung der quantitativen phytoplankton-methodik. (The improvement of quantitative phytoplankton methodology. In German.) Mitt. Internat. Verein. Limnol., 9: 1–38.
Verity, P. G., Robertson, C. Y., Tronzo, C. R., Andrews, M. G., Nelson, J. R. and Sieracki, M. E. 1992. Relationship between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol. Oceanogr., 37: 1434–1446.
Vollenweider, R. A., Munawar, M. and Stadelmann, P. 1974. A comparative review of phytoplankton and primary production in the Laurentian Great Lakes. J. Fish. Res. Board Can., 31: 739–762.
Walsh, M. G., O’Gorman, R., Strang, T., Edwards, W. H. and Rudstam, L. G. 2008. Fall diets of alewife, rainbow smelt, and slimy sculpin in the profundal zone of southern Lake Ontario during 1994–2005 with an emphasis on occurrence of Mysis relicta. Aquat. Ecosyst. Health. Mgmt., 11(4): 368–376.
Weisse, T. 1997. Growth and production of heterotrophic nanoflagellates in a meso-eutrophic lake. J. Plankton Res., 19(6): 703–722.
Published
Issue
Section
License
Manuscripts must be original. They must not be published or be under consideration for publication elsewhere, in whole or in part. It is required that the lead author of accepted papers complete and sign the MSU Press AEHM Author Publishing Agreement and provide it to the publisher upon acceptance.
